Subdivisions of primary motor cortex based on cortico-motoneuronal cells - PubMed (original) (raw)

Subdivisions of primary motor cortex based on cortico-motoneuronal cells

Jean-Alban Rathelot et al. Proc Natl Acad Sci U S A. 2009.

Abstract

We used retrograde transneuronal transport of rabies virus from single muscles of rhesus monkeys to identify cortico-motoneuronal (CM) cells in the primary motor cortex (M1) that make monosynaptic connections with motoneurons innervating shoulder, elbow, and finger muscles. We found that M1 has 2 subdivisions. A rostral region lacks CM cells and represents an "old" M1 that is the standard for many mammals. The descending commands mediated by corticospinal efferents from old M1 must use the integrative mechanisms of the spinal cord to generate motoneuron activity and motor output. In contrast, a caudal region of M1 contains shoulder, elbow, and finger CM cells. This region represents a "new" M1 that is present only in some higher primates and humans. The direct access to motoneurons afforded by CM cells enables the newly recognized M1 to bypass spinal cord mechanisms and sculpt novel patterns of motor output that are essential for highly skilled movements.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Fig. 1.

Distribution of CM cells innervating the motoneurons of a shoulder or an elbow muscle. (Upper) Results from injections of rabies into the SpD muscle. (Lower) Results from injections into the lateral head of the lTri muscle. Each map shows an unfolded reconstruction of layer V from an experimental case. Each dot represents a labeled CM cell. In this and other figures, the vertical dashed line in each map represents the edge of the CS, and vertical dotted lines indicate the approximate location of cytoarchitectonic borders. The central Inset shows the general location of the reconstructed area on a lateral view of the macaque cerebral hemisphere. Note that most shoulder and elbow CM cells are located medially in the CS. ArS, arcuate sulcus; C, caudal; M, medial; Gyrus, crest of the precentral gyrus; Sulcus, anterior bank of the CS.

Fig. 2.

Fig. 2.

Overlap maps of CM cells innervating proximal versus distal muscles. (A) Black dots represent CM cells labeled by injections into SpD (n = 2). (B) Black dots represent CM cells labeled by injections into lTri (n = 2). Gray dots in A and B represent CM cells labeled after virus injections into finger muscles (ADP or ABPL) (from figure 3 in ref. 2). Note that some elbow and shoulder CM cells are found in regions of the CS where there is a high density of finger CM cells.

Fig. 3.

Fig. 3.

Topographic organization of CM cells in M1. (Upper) Density analysis of CM cells innervating shoulder (Left), elbow (Center), or finger (Right) motoneurons. The color scale at the right indicates the density of labeled neurons as percentages relative to the maximum peak density. Note the presence of a large medial group of shoulder CM cells along with a small lateral group. (Lower) (Left) Density peaks of shoulder (white), elbow (blue), and finger (red) CM cells. The cutoff for shoulder and finger CM cells, upper 75%; the cutoff for elbow CM cells, upper 87.5%. Note that in general the peak densities of shoulder and elbow CM cells are located medial to the peak density of finger CM cells. Even so, there is considerable intermingling of the different populations of CM cells. (Right) Results of intracortical stimulation (redrawn from ref. with permission of the American Physiological Society). Colors indicate the movement evoked by threshold stimulation at each site: shoulder (white), elbow (blue), or finger (red). Symbol size indicates the threshold for each site (key below). In the CS, most shoulder and elbow sites were located medial to finger sites. However, a small number of high threshold shoulder and elbow sites were located more laterally in the CS. Compare the location of these sites with the small lateral group of shoulder CM cells shown in Upper Left.

Fig. 4.

Fig. 4.

Correspondence between CM cells and low threshold sites. (A) Map of all CM cells (yellow dots) labeled by rabies injections into shoulder (SpD), elbow (lTri), and finger (ABPL, ADP, and EDC) muscles. The map is an overlap of the data presented in Fig. 1 and the data presented in figure 3 in ref. . (B) Plot of sites where intracortical microstimulation at the lowest threshold (2–5 μA) evoked shoulder (white), elbow (blue), and finger (red) movements (data from ref. 3). Note that the lowest threshold sites for evoking movement and CM cells are most concentrated in the caudal portion of M1 in the CS.

Fig. 5.

Fig. 5.

Third-order neurons in motor cortex. We injected rabies virus into the ABPL muscle, and the survival time was set to allow labeling of third-order neurons (experiment JA29 in

Table S2

). (A) Plot of a sagittal section (300) through M1 showing labeled neurons (dots). Layer V is shaded gray. (B) Map of labeled neurons in layer III. (C) Map of labeled neurons in layer V. The location of section 300 is indicated on the maps by horizontal arrows. C, caudal; D, dorsal; M, medial; SPcS, superior precentral sulcus. Note that third-order neurons in layer III are largely confined to the caudal portion of M1 in the CS, whereas layer V neurons (second- and third-order) are found in rostral as well as caudal portions of M1.

Fig. 6.

Fig. 6.

New and old M1. New M1 is located caudally in the CS and has CM cells that make direct connections with motoneurons. In contrast, old M1 is located rostrally on the precentral gyrus and lacks CM cells. However, old M1 has CST neurons that influence motoneurons indirectly through their connections with spinal interneurons. CM, cortico-motoneuronal; CST, corticospinal; In, interneurons; Mn, motoneurons.

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